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Review
. 2002;10(1-2):17-39.

Small nucleolar RNAs: versatile trans-acting molecules of ancient evolutionary origin

Michael P Terns  1 , Rebecca M Terns
Affiliations
Review

Small nucleolar RNAs: versatile trans-acting molecules of ancient evolutionary origin

Michael P Terns et al. Gene Expr. 2002.

Abstract

The small nucleolar RNAs (snoRNAs) are an abundant class of trans-acting RNAs that function in ribosome biogenesis in the eukaryotic nucleolus. Elegant work has revealed that most known snoRNAs guide modification of pre-ribosomal RNA (pre-rRNA) by base pairing near target sites. Other snoRNAs are involved in cleavage of pre-rRNA by mechanisms that have not yet been detailed. Moreover, our appreciation of the cellular roles of the snoRNAs is expanding with new evidence that snoRNAs also target modification of small nuclear RNAs and messenger RNAs. Many snoRNAs are produced by unorthodox modes of biogenesis including salvage from introns of pre-mRNAs. The recent discovery that homologs of snoRNAs as well as associated proteins exist in the domain Archaea indicates that the RNA-guided RNA modification system is of ancient evolutionary origin. In addition, it has become clear that the RNA component of vertebrate telomerase (an enzyme implicated in cancer and cellular senescence) is related to snoRNAs. During its evolution, vertebrate telomerase RNA appears to have co-opted a snoRNA domain that is essential for the function of telomerase RNA in vivo. The unique properties of snoRNAs are now being harnessed for basic research and therapeutic applications.

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Figures

Figure 1
Figure 1
snoRNAs mark rRNA sites for modification. (A) Box C/D guide RNAs direct site-specific rRNA 2′-O-ribose methylation. A box C/ D snoRNA (black) base pairs with one or two complementary rRNA sequences (gray) via complementary sequences (guide sequences) found upstream of box D and/or box D′. The 2′-O-methyl group (M) is always added to the rRNA nucleotide that is paired to the fifth residue upstream of the conserved box D and/or box D′ element. The box C/D motif, a common feature of box C/D snoRNAs, is shaded. (B) Box H/ACA guide RNAs direct the conversion of uridines to pseudouridines. A box H/ACA snoRNA (black) base pairs with complementary rRNA sequences (gray) in one or two loop regions (“pseudouridine pockets”). The target uridine(s) (Ψ) remain unpaired. Pseudouridine formation takes place∼15 nucleotides from the conserved box H or box ACA element. The box H/ACA motif, a common feature of box H/ACA snoRNAs, is shaded.
Figure 2
Figure 2
Structure–function analysis of box C/D snoRNAs. (A) U3 snoRNA (the most extensively analyzed box C/D snoRNA) contains five conserved sequence elements known as boxes A′, A, C′, B, C, and D as well as a “hinge” region (H). Box A′, box A, and the hinge each participate in U3 snoRNA/rRNA base pairing. Boxes B and C, and boxes C′ and D form functional units called the box B/C motif (U3 specific) and the box C′/D motif (common to other box C/D snoRNAs). A terminal stem (TS) is a critical component of the box C′/D motif of U3. The functions of the box B/C motif and the box C′/D motif elucidated by mutational analysis are indicated (see text for details). (B) The box C/D motif is a common feature of box C/D RNAs. The indicated properties of the box C/D motif have been inferred from studies of minimal RNAs comprised essentially of the box C/D motif (box C and box D separated by intervening sequences and linked by a terminal stem). †W. Speckmann, R. M. Terns, and M. P. Terns, unpublished data.
Figure 3
Figure 3
Relationships between the known protein components of box C/D and box H/ACA RNPs in eukaryotes, and homologous proteins encoded in archaeal genomes. Only fibrillarin and Nop56/ 58 have been experimentally determined to be associated with box C/D RNAs in archaea (153). Three pairs of eukaryotic snoRNP protein genes are represented by a single gene in archaea: Nop56 and Nop58 (140), p50 and p55 (140), and Snu13 and Nhp2 (R. M. Terns and M. P. Terns, see text). The archaeal Nop56/58 protein is also related to Prp31 (73). The archaeal Snu13/Nhp2 protein is also related to ribosomal protein RPL8 or L7a (R. M. Terns and M. P. Terns, see text). See text for additional details.
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